State-dependent decoupling of sensory and motor circuits underlies behavioral flexibility in Drosophila

Abstract

An approaching predator and self-motion towards an object can generate similar looming patterns on the retina, but these situations demand different rapid responses. How central circuits flexibly process visual cues to activate appropriate, fast motor pathways remains unclear. Here, we identify two descending neuron (DN) types that control landing and contribute to visuomotor flexibility in Drosophila . For each, silencing impairs visually-evoked landing, activation drives landing, and spike rate determines leg extension amplitude. Critically, visual responses of both DNs are severely attenuated during non-flight periods, effectively decoupling visual stimuli from the landing motor pathway when landing is inappropriate. The flight-dependence mechanism differs between DN types. Octopamine exposure mimics flight effects in one, whereas the other likely receives neuronal feedback from flight motor circuits. Thus, this sensorimotor flexibility arises from distinct mechanisms for gating action-specific descending pathways, such that sensory and motor networks are coupled or decoupled according to the behavioral state.

Neural circuit mechanisms for steering control in walkingDrosophila

“…10). Similarly, a recent study found that Drosophila DNs that evoke landing during flight are still responsive to visual stimuli when the fly is not flying 45 . We might think of these residual DN responses as a latent bias toward action, or a preparation for an action that never ultimately occurs 46 .…”

Facilitation of neural responses to targets moving against optic flow

“…It is possible that the TSDN responses that we recorded are affected by the animals being immobilized. Indeed, in two descending neurons types that control landing behaviors in Drosophila , visual responses are suppressed in non-flight states 52 . Octopamine, which has been shown to mimic flight behavior, restores responses in one of these neurons, while the other may receive direct feedback from flight motor circuits 52 .…”

An unbiased template of theDrosophilabrain and ventral nerve cord

“…A block-based storage scheme would incur less overhead because it enables efficient access of subset of the displacement field data. HDF5 ("h5") is a popular and ubiquitous choice for such storage needs (The HDF Group, 1997-2019.…”

“…While studies of the Drosophila ventral nerve cord (VNC) are numerous and ongoing (Prokop and Technau, 1991;Stockinger et al, 2005;Lacin and Truman, 2016;Ache et al, 2019), efforts in generating a standard anatomical coordinate system are somewhat lacking. Börner and Duch (2010) created a standard Drosophila VNC, but to our knowledge, the data are not publicly available; thus its impact is limited.…”